Acridine Orange/exosomes increase the delivery and the effectiveness of Acridine Orange in human melanoma cells: A new prototype for theranostics of tumors

References

• Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 2005;5:516–25.
   PubMed Web of Science ®Google Scholar
• Stavreva NA, Stavrev PV, Warkentin B, Fallone BG. Investigating the effect of cell repopulation on the tumor response to fractionated external radiotherapy. Med Phys 2003;30:735–42.
   PubMed Web of Science ®Google Scholar
• Brade AM, Tannock IF. Scheduling of radiation and chemotherapy for limited-stage small-cell lung cancer: repopulation as a cause of treatment failure? J Clin Oncol 2006;24:1020–2.
   PubMed Web of Science ®Google Scholar
• Davis AJ, Tannock JF. Repopulation of tumour cells between cycles of chemotherapy: a neglected factor. Lancet Oncol 2000;1:86–93.
   PubMedGoogle Scholar
• Corry J, Rischin D. Strategies to overcome accelerated repopulation and hypoxia-what have we learned from clinical trials? Semin Oncol 2004;31:802–8.
   PubMed Web of Science ®Google Scholar
• Vassileva V, Allen CJ, Piquette-Miller M. Effects of sustained and intermittent paclitaxel therapy on tumor repopulation in ovarian cancer. Mol Cancer Ther 2008;7:630.
   PubMed Web of Science ®Google Scholar
• Leung M, Florendo J, Kano J, et al. A modified filgrastim regimen does not reduce pain burden compared to pegfilgrastim in women receiving chemotherapy for non-metastatic breast cancer. Support Care Cancer 2015;23:1669–77.
   PubMed Web of Science ®Google Scholar
• Zuo RC, Apolo AB, DiGiovanna JJ, et al. Cutaneous adverse effects associated with the tyrosine-kinase inhibitor cabozantinib. JAMA Dermatol 2015;151:170–7.
   PubMed Web of Science ®Google Scholar
• Handforth C, Clegg A, Young C, et al. The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann Oncol 2015;26:1091–101.
   PubMed Web of Science ®Google Scholar
• Au JL, Jang SH, Zheng J, et al. Determinants of drug delivery and transport to solid tumors. J Control Release 2001;74:31–46.
   PubMed Web of Science ®Google Scholar
• Au JL, Jang SH, Wientjes MG. Clinical aspects of drug delivery to tumors. J Control Release 2002;78:81–95.
   PubMed Web of Science ®Google Scholar
• Jang SH, Wientjes MG, Lu D, Au JLS. Drug delivery and transport to solid tumors. Pharm Res 2003;20:1337–50.
   PubMed Web of Science ®Google Scholar
• Spugnini EP, Sonveaux P, Stock C, et al. Proton channels and exchangers in cancer. Biochim Biophys Acta 2015;1848:2715–26.
   PubMed Web of Science ®Google Scholar
• Fais S, Venturi G, Gatenby B. Microenvironmental acidosis in carcinogenesis and metastases: new strategies in prevention and therapy. Cancer Met Rev 2014;33:1095–108.
   PubMed Web of Science ®Google Scholar
• Bailey KM, Wojtkowiak JW, Hashim AI, Gillies RJ. Targeting the metabolic microenvironment of tumors. Adv Pharmacol 2012;65:63–107.
   PubMedGoogle Scholar
• Mahoney BP, Raghunand N, Baggett B, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 2003;66:1207–18.
   PubMed Web of Science ®Google Scholar
• Raghunand N, Mahoney BP, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. II. pH dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol 2003;66:1219–29.
   PubMed Web of Science ®Google Scholar
• Azzarito T, Venturi G, Cesolini A, Fais S. Lansoprazole induces sensitivity to suboptimal doses of paclitaxel in human melanoma. Cancer Lett 2015;356:697–703.
   PubMed Web of Science ®Google Scholar
• Luciani F, Spada M, De Milito A, et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst 2004;96:1702–13.
   PubMed Web of Science ®Google Scholar
• Taylor S, Spugnini EP, Assaraf YG, et al. Microenvironment acidity as a major determinant of tumor chemoresistance: proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updat 2015;23:69–78.
   PubMed Web of Science ®Google Scholar
• De Milito A, Iessi E, Logozzi M, et al. Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspase-independent mechanism involving reactive oxygen species. Cancer Res 2007;67:5408–17.
   PubMed Web of Science ®Google Scholar
• De Milito A, Canese R, Marino ML, et al. pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity. Int J Cancer 2010;127:207–19.
   PubMed Web of Science ®Google Scholar
• Lugini L, Federici C, Borghi M, et al. Proton pump inhibitors while belonging to the same family of generic drugs show different anti-tumor effect. J Enzyme Inhib Med Chem 2016;31:538–45.
   PubMed Web of Science ®Google Scholar
• Canitano A, Iessi E, Spugnini EP, et al. Proton pump inhibitors induce a caspase-independent antitumor effect against human multiple myeloma. Cancer Lett 2016;376:278–83.
   PubMed Web of Science ®Google Scholar
• Fais S. Proton pump inhibitor-induced tumour cell death by inhibition of a detoxification mechanism. J Intern Med 2010;267:515–25.
   PubMed Web of Science ®Google Scholar
• Fais S, De Milito A, You H, Qin W. Targeting vacuolar H+-ATPases as a new strategy against cancer. Cancer Res 2007;67:10627–30.
   PubMed Web of Science ®Google Scholar
• You H, Jin J, Shu H, et al. Small interfering RNA targeting the subunit ATP6L of proton pump V-ATPase overcomes chemoresistance of breast cancer cells. Cancer Lett 2009;280:110–19.
   PubMed Web of Science ®Google Scholar
• Ferrari S, Perut F, Fagioli F, et al. Proton pump inhibitor chemosensitization in human osteosarcoma: from the bench to the patients' bed. J Transl Med 2013;11:268.
   PubMed Web of Science ®Google Scholar
• Wang BY, Zhang J, Wang JL, et al. Erratum to: intermittent high dose proton pump inhibitor enhances the antitumor effects of chemotherapy in metastatic breast cancer. J Exp Clin Cancer Res 2015;34:109.
   PubMed Web of Science ®Google Scholar
• Spugnini EP, Baldi A, Buglioni S, et al. Lansoprazole as a rescue agent in chemoresistant tumors: a phase I/II study in companion animals with spontaneously occurring tumors. J Transl Med 2011;9:221.
   PubMed Web of Science ®Google Scholar
• Spugnini EP, Buglioni S, Carocci F, et al. High dose lansoprazole combined with metronomic chemotherapy: a phase I/II study in companion animals with spontaneously occurring tumors. J Transl Med 2014;12:225.
   PubMed Web of Science ®Google Scholar
• Fais S. Evidence-based support for the use of proton pump inhibitors in cancer therapy. J Transl Med 2015;13:368.
   PubMed Web of Science ®Google Scholar
• Huber V, De Milito A, Harguindey S, et al. Proton dynamics in cancer. J Transl Med 2010;8:57.
   PubMed Web of Science ®Google Scholar
• Kusuzaki K, Hosogi S, Ashihara E, et al. Translational research of photodynamic therapy with acridine orange which targets cancer acidity. Curr Pharm Des 2012;18:1414–20.
   PubMed Web of Science ®Google Scholar
• Zelenin AV. Fluorescence microscopy of lysosomes and related structures in living cells. Nature 1966;212:425–6.
   PubMed Web of Science ®Google Scholar
• Zdolsek JM, Olsson GM, Brunk UT. Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem Photobiol 1990;51:67–76.
   PubMed Web of Science ®Google Scholar
• Webb SD, Sherratt JA, Fish RG. Mathematical modelling of tumour acidity: regulation of intracellular pH. J Theor Biol 1999;196:237–50.
   PubMed Web of Science ®Google Scholar
• Hiruma H, Katakura T, Takenami T, et al. Vesicle disruption, plasma membrane bleb formation, and acute cell death caused by illumination with blue light in acridine orange-loaded malignant melanoma cells. J Photochem Photobiol B 2007;86:1–8.
   PubMed Web of Science ®Google Scholar
• Satonaka H, Kusuzaki K, Matsubara T, et al. Extracorporeal photodynamic image detection of mouse osteosarcoma in soft tissues utilizing fluorovisualization effect of acridine orange. Oncology 2006;70:465–73.
   PubMed Web of Science ®Google Scholar
• Satonaka H, Kusuzaki K, Matsubara T, et al. Flash wave light strongly enhanced the cytocidal effect of photodynamic therapy with acridine orange on a mouse osteosarcoma cell line. Anticancer Res 2007;27:3339–44.
   PubMed Web of Science ®Google Scholar
• Satonaka H, Kusuzaki K, Matsubara T, et al. In vivo anti-tumor activity of photodynamic therapy with intravenous administration of acridine orange, followed by illumination with high-power flash wave light in a mouse osteosarcoma model. Oncol Lett 2010;1:69–72.
   PubMed Web of Science ®Google Scholar
• Yoshida K, Kusuzaki K, Matsubara T, et al. Periosteal Ewing's sarcoma treated by photodynamic therapy with acridine orange. Oncol Rep 2005;13:279–82.
   PubMed Web of Science ®Google Scholar
• Kusuzaki K, Murata H, Matsubara T, et al. Clinical outcome of a novel photodynamic therapy technique using acridine orange for synovial sarcomas. Photochem Photobiol 2005;81:705–9.
   PubMed Web of Science ®Google Scholar
• Kusuzaki K, Murata H, Matsubara T, et al. Clinical trial of photodynamic therapy using acridine orange with/without low dose radiation as new limb salvage modality in musculoskeletal sarcomas. Anticancer Res 2005;25:1225–35.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Kusuzaki K, Matsubara T, et al. A new limb salvage surgery in cases of high-grade soft tissue sarcoma using photodynamic surgery, followed by photo- and radiodynamic therapy with acridine orange. J Surg Oncol 2008;97:523–8.
   PubMed Web of Science ®Google Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. A new therapeutic modality involving acridine orange excitation by photon energy used during reduction surgery for rhabdomyosarcomas. Oncol Rep 2009;21:89–94.
   PubMed Web of Science ®Google Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. Photodynamic therapy with acridine orange in musculoskeletal sarcomas. J Bone Joint Surg Br 2010;92:760–2.
   PubMedGoogle Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. Clinical outcomes of minimally invasive surgery using acridine orange for musculoskeletal sarcomas around the forearm, compared with conventional limb salvage surgery after wide resection. J Surg Oncol 2010;102:271–5.
   PubMed Web of Science ®Google Scholar
• Matsubara T, Kusuzaki K, Matsumine A, et al. Acridine orange used for photodynamic therapy accumulates in malignant musculoskeletal tumors depending on pH gradient. Anticancer Res 2006;26:187–93.
   PubMed Web of Science ®Google Scholar
• Hashiguchi S, Kusuzaki K, Murata H, et al. Acridine orange excited by low-dose radiation has a strong cytocidal effect on mouse osteosarcoma. Oncology 2002;62:85–93.
   PubMed Web of Science ®Google Scholar
• Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569–79.
   PubMed Web of Science ®Google Scholar
• Jang SC, Kim OY, Yoon CM, et al. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano 2013;7:7698–710.
   PubMed Web of Science ®Google Scholar
• Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 2014;35:2383–90.
   PubMed Web of Science ®Google Scholar
• Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 2011;29:341–5.
   PubMed Web of Science ®Google Scholar
• El-Andaloussi S, Lee Y, Lakhal-Littleton S, et al. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc 2012;7:2112–26.
   PubMed Web of Science ®Google Scholar
• Foglio E, Puddighinu G, Fasanaro P, et al. Exosomal clusterin, identified in the pericardial fluid, improves myocardial performance following MI through epicardial activation, enhanced arteriogenesis and reduced apoptosis. Int J Cardiol 2015;197:333–47.
   PubMed Web of Science ®Google Scholar
• Fais S, O'Driscoll L, Borras FE, et al. Evidence-based clinical use of nanoscale extracellular vesicles in nanomedicine. ACS Nano 2016;10:3886–99.
   PubMed Web of Science ®Google Scholar
• Campanella C, Rappa F, Sciumè C, et al. Heat shock protein 60 levels in tissue and circulating exosomes in human large bowel cancer before and after ablative surgery. Cancer 2015;121:3230–9.
   PubMed Web of Science ®Google Scholar
• Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015;4:27066.
   PubMed Web of Science ®Google Scholar
• Properzi F, Logozzi M, Abdel-Haq H, et al. Detection of exosomal prions in blood by immunochemistry techniques. J Gen Virol 2015;96:1969–74.
   PubMed Web of Science ®Google Scholar
• Zocco D, Ferruzzi P, Cappello F, et al. Extracellular vesicles as shuttles of tumor biomarkers and anti-tumor drugs. Front Oncol 2014;4:267.
   PubMedGoogle Scholar
• Cossetti C, Lugini L, Astrologo L, et al. Soma-to-germline transmission of RNA in mice xenografted with human tumour cells: possible transport by exosomes. PLoS One 2014;9:e101629.
   PubMed Web of Science ®Google Scholar
• Federici C, Petrucci F, Caimi S, et al. Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS One 2014;9:e88193.
   PubMed Web of Science ®Google Scholar
• Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med 2013;7:769–78.
   PubMed Web of Science ®Google Scholar
• Fais S. NK cell-released exosomes: natural nanobullets against tumors. Oncoimmunology 2013;2:e22337.
   PubMed Web of Science ®Google Scholar
• Fais S, Logozzi M, Lugini L, et al. Exosomes: the ideal nanovectors for biodelivery. Biol Chem 2013;394:1–15.
   PubMed Web of Science ®Google Scholar
• Lugini L, Cecchetti S, Huber V, et al. Immune surveillance properties of human NK cell-derived exosomes. J Immunol 2012;189:2833–42.
   PubMed Web of Science ®Google Scholar
• Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009;284:34211–22.
   PubMed Web of Science ®Google Scholar
• Lener T, Gimona M, Aigner L, et al. Applying extracellular vesicles based therapeutics in clinical trials – an ISEV position paper. J Extracell Vesicles 2015;4:30087.
   PubMed Web of Science ®Google Scholar
• Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006; Chapter 3: Unit3.22.
   PubMedGoogle Scholar
• Hunger RE, Angermeier S, Seyed Jafari SM, et al. A retrospective study of 1- versus 2-cm excision margins for cutaneous malignant melanomas thicker than 2 mm. J Am Acad Dermatol 2015;72:1054–9.
   PubMed Web of Science ®Google Scholar
• Speijers MJ, Bastiaannet E, Sloot S, et al. Tumor mitotic rate added to the equation: melanoma prognostic factors changed? A single-institution database study on the prognostic value of tumor mitotic rate for sentinel lymph node status and survival of cutaneous melanoma patients. Ann Surg Oncol 2015;22:2978–87.
   PubMed Web of Science ®Google Scholar
• Melstrom LG, Taylor E, Kuk D, et al. International multi-institutional management and outcome of melanoma patients with positive sentinel lymph nodes in more than one nodal basin. Ann Surg Oncol 2014;21:4324–9.
   PubMed Web of Science ®Google Scholar
• Saco M, Thigpen J. A retrospective comparison between preoperative and postoperative Breslow depth in primary cutaneous melanoma: how preoperative shave biopsies affect surgical management. J Drugs Dermatol 2014;13:531–6.
   PubMed Web of Science ®Google Scholar
• Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277–300.
   PubMed Web of Science ®Google Scholar
• Bandarchi B, Ma L, Navab R, et al. From melanocyte to metastatic malignant melanoma. Dermatol Res Pract 2010;2010:583748.
   PubMedGoogle Scholar
• Bristow BN, Casil J, Sorvillo F, et al. Melanoma-related mortality and productivity losses in the USA, 1990–2008. Melanoma Res 2013;23:331–5.
   PubMed Web of Science ®Google Scholar
• Bhatia S, Tykodi SS, Thompson JA. Treatment of metastatic melanoma: an overview. Oncology (Williston Park, NY) 2009;23:488–96.
   PubMed Web of Science ®Google Scholar
• Fais S. A nonmainstream approach against cancer. J Enzyme Inhib Med Chem 2016;31:882–9.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Kusuzaki K, Matsubara T, et al. Determination of the LD50 of acridine orange via intravenous administration in mice in preparation for clinical application to cancer therapy. In Vivo 2014;28:523–8.
   PubMed Web of Science ®Google Scholar
• Satonaka H, Kusuzaki K, Akeda K, et al. Acridine orange inhibits pulmonary metastasis of mouse osteosarcoma. Anticancer Res 2011;31:4163–8.
   PubMed Web of Science ®Google Scholar